Home LiteratureArticle Details
PMID: 20153629 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review

New functions for an old variant: no substitute for histone H3.3.

Current opinion in genetics & development ·Vol. 20 ·No. 2 ·2010-04-00 ·Pages 110-7

Elsaesser SJ, Goldberg AD, Allis CD

Abstract

Histone proteins often come in different variants serving specialized functions in addition to their fundamental role in packaging DNA. The metazoan histone H3.3 has been most closely associated with active transcription. Its role in histone replacement at active genes and promoters is conserved to the single histone H3 in yeast. However, recent genetic studies in flies have challenged its importance as a mark of active chromatin, and revealed unexpected insights into essential functions of H3.3 in the germline. With strikingly little amino acid sequence difference to the canonical H3, H3.3 therefore accomplishes a surprising variety of cellular and developmental processes.

MeSH Terms
Animals Cell Cycle/physiology Chromatin/metabolism Chromatin Assembly and Disassembly/physiology Epigenesis, Genetic Gene Expression Regulation, Developmental Genetic Variation Histones/genetics,metabolism,physiology Humans Reproduction/physiology
Chemicals
Chromatin Histones
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Elsaesser Simon J
The Rockefeller University, New York, NY 10065, USA. selsaesser@rockefeller.edu <selsaesser@rockefeller.edu>
Goldberg Aaron D
Allis C David
References (66)
66 references, click to expand
  1. H3.3/H2A.Z double variant-containing nucleosomes mark 'nucleosome-free regions' of active promoters and other regulatory regions.
    Nat Genet. 2009 Aug;41(8):941-5 PMID: 19633671
  2. The Schizosaccharomyces pombe HIRA-like protein Hip1 is required for the periodic expression of histone genes and contributes to the function of complex centromeres.
    Mol Cell Biol. 2004 May;24(10):4309-20 PMID: 15121850
  3. Dynamic histone variant exchange accompanies gene induction in T cells.
    Mol Cell Biol. 2009 Apr;29(7):1972-86 PMID: 19158270
  4. Genome-wide replication-independent histone H3 exchange occurs predominantly at promoters and implicates H3 K56 acetylation and Asf1.
    Mol Cell. 2007 Aug 3;27(3):393-405 PMID: 17679090
  5. Transcriptional activators are dispensable for transcription in the absence of Spt6-mediated chromatin reassembly of promoter regions.
    Mol Cell. 2006 Feb 3;21(3):405-16 PMID: 16455495
  6. HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis.
    Mol Cell. 2002 May;9(5):1091-100 PMID: 12049744
  7. The essential role of Drosophila HIRA for de novo assembly of paternal chromatin at fertilization.
    PLoS Genet. 2007 Oct;3(10):1991-2006 PMID: 17967064
  8. Variant histone H3.3 is deposited at sites of nucleosomal displacement throughout transcribed genes while active histone modifications show a promoter-proximal bias.
    Genes Dev. 2005 Aug 1;19(15):1761-6 PMID: 16077006
  9. Evidence that Spt6p controls chromatin structure by a direct interaction with histones.
    Science. 1996 Jun 7;272(5267):1473-6 PMID: 8633238
  10. Serine 31 phosphorylation of histone variant H3.3 is specific to regions bordering centromeres in metaphase chromosomes.
    Proc Natl Acad Sci U S A. 2005 May 3;102(18):6344-9 PMID: 15851689
  11. The HIR corepressor complex binds to nucleosomes generating a distinct protein/DNA complex resistant to remodeling by SWI/SNF.
    Genes Dev. 2005 Nov 1;19(21):2534-9 PMID: 16264190
  12. Histone chaperones regulate histone exchange during transcription.
    EMBO J. 2007 Oct 31;26(21):4467-74 PMID: 17914459
  13. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis.
    Cell. 2004 Jan 9;116(1):51-61 PMID: 14718166
  14. A 17-kD centromere protein (CENP-A) copurifies with nucleosome core particles and with histones.
    J Cell Biol. 1987 Apr;104(4):805-15 PMID: 3558482
  15. Regulation of histone mRNA in the unperturbed cell cycle: evidence suggesting control at two posttranscriptional steps.
    Mol Cell Biol. 1991 May;11(5):2416-24 PMID: 2017161
  16. Potential role of the histone chaperone, CAF-1, in transcription.
    BMB Rep. 2009 Apr 30;42(4):227-31 PMID: 19403047
  17. Non-allelic variants of histones 2a, 2b and 3 in mammals.
    Nature. 1977 Mar 17;266(5599):273-5 PMID: 846573
  18. Histone dynamics in living cells revealed by photobleaching.
    DNA Repair (Amst). 2005 Jul 28;4(8):939-50 PMID: 15905138
  19. Human UBN1 is an ortholog of yeast Hpc2p and has an essential role in the HIRA/ASF1a chromatin-remodeling pathway in senescent cells.
    Mol Cell Biol. 2009 Feb;29(3):758-70 PMID: 19029251
  20. Dynamics of replication-independent histone turnover in budding yeast.
    Science. 2007 Mar 9;315(5817):1405-8 PMID: 17347438
  21. Two types of polyadenated mRNAs are synthesized from Drosophila replication-dependent histone genes.
    Eur J Biochem. 1997 Mar 1;244(2):294-300 PMID: 9118993
  22. H2A.Z and H3.3 histone variants affect nucleosome structure: biochemical and biophysical studies.
    Biochemistry. 2009 Nov 24;48(46):10852-7 PMID: 19856965
  23. Molecular dissection of formation of senescence-associated heterochromatin foci.
    Mol Cell Biol. 2007 Mar;27(6):2343-58 PMID: 17242207
  24. Differential regulation of repeated histone genes during the fission yeast cell cycle.
    Nucleic Acids Res. 2007;35(10):3223-37 PMID: 17452352
  25. Histone H1 binding is inhibited by histone variant H3.3.
    EMBO J. 2009 Dec 2;28(23):3635-45 PMID: 19834459
  26. Dynamic regulation of replication independent deposition of histone H3 in fission yeast.
    Nucleic Acids Res. 2005 Dec 15;33(22):7102-10 PMID: 16361268
  27. Patterns of histone variant synthesis can distinguish G0 from G1 cells.
    Cell. 1982 Dec;31(2 Pt 1):367-74 PMID: 7159927
  28. Chromosome-wide nucleosome replacement and H3.3 incorporation during mammalian meiotic sex chromosome inactivation.
    Nat Genet. 2007 Feb;39(2):251-8 PMID: 17237782
  29. Dynamic distribution of the replacement histone variant H3.3 in the mouse oocyte and preimplantation embryos.
    Int J Dev Biol. 2006;50(5):455-61 PMID: 16586346
  30. Replication-independent histone deposition by the HIR complex and Asf1.
    Curr Biol. 2005 Nov 22;15(22):2044-9 PMID: 16303565
  31. Formation of the 3' end of histone mRNA.
    Gene. 1999 Oct 18;239(1):1-14 PMID: 10571029
  32. From silencing to gene expression: real-time analysis in single cells.
    Cell. 2004 Mar 5;116(5):683-98 PMID: 15006351
  33. Histone H3.3 deposition at E2F-regulated genes is linked to transcription.
    EMBO Rep. 2006 Jan;7(1):66-71 PMID: 16258499
  34. Histone H3.3 incorporation provides a unique and functionally essential telomeric chromatin in embryonic stem cells.
    Genome Res. 2009 Mar;19(3):404-14 PMID: 19196724
  35. Defects in SPT16 or POB3 (yFACT) in Saccharomyces cerevisiae cause dependence on the Hir/Hpc pathway: polymerase passage may degrade chromatin structure.
    Genetics. 2002 Dec;162(4):1557-71 PMID: 12524332
  36. The histone chaperone Asf1p mediates global chromatin disassembly in vivo.
    J Biol Chem. 2004 Dec 10;279(50):52069-74 PMID: 15452122
  37. Continuous histone H2B and transcription-dependent histone H3 exchange in yeast cells outside of replication.
    Mol Cell. 2007 Feb 9;25(3):345-55 PMID: 17289583
  38. Variant histone H3.3 marks promoters of transcriptionally active genes during mammalian cell division.
    EMBO Rep. 2005 Apr;6(4):354-60 PMID: 15776021
  39. Histones are incorporated in trans during reassembly of the yeast PHO5 promoter.
    Mol Cell. 2005 Jul 22;19(2):279-85 PMID: 16039596
  40. A retroviral gene trap insertion into the histone 3.3A gene causes partial neonatal lethality, stunted growth, neuromuscular deficits and male sub-fertility in transgenic mice.
    Hum Mol Genet. 1999 Dec;8(13):2489-95 PMID: 10556297
  41. Two-color cell array screen reveals interdependent roles for histone chaperones and a chromatin boundary regulator in histone gene repression.
    Mol Cell. 2009 Aug 14;35(3):340-51 PMID: 19683497
  42. Histone replacement marks the boundaries of cis-regulatory domains.
    Science. 2007 Mar 9;315(5817):1408-11 PMID: 17347439
  43. Yeast histone deposition protein Asf1p requires Hir proteins and PCNA for heterochromatic silencing.
    Curr Biol. 2001 Apr 3;11(7):463-73 PMID: 11412995
  44. Characterization of HIR1 and HIR2, two genes required for regulation of histone gene transcription in Saccharomyces cerevisiae.
    Mol Cell Biol. 1993 Jan;13(1):28-38 PMID: 8417331
  45. Inducible deposition of the histone variant H3.3 in interferon-stimulated genes.
    J Biol Chem. 2009 May 1;284(18):12217-25 PMID: 19244243
  46. SWI/SNF and Asf1p cooperate to displace histones during induction of the saccharomyces cerevisiae HO promoter.
    Mol Cell Biol. 2009 Aug;29(15):4057-66 PMID: 19470759
  47. Histone variants specific to the transcriptionally active, amitotically dividing macronucleus of the unicellular eucaryote, Tetrahymena thermophila.
    Cell. 1980 Jul;20(3):609-17 PMID: 7418000
  48. Transcriptional activation triggers deposition and removal of the histone variant H3.3.
    Genes Dev. 2005 Apr 1;19(7):804-14 PMID: 15774717
  49. Targeted mutagenesis of the Hira gene results in gastrulation defects and patterning abnormalities of mesoendodermal derivatives prior to early embryonic lethality.
    Mol Cell Biol. 2002 Apr;22(7):2318-28 PMID: 11884616
  50. Molecular evolution of the nontandemly repeated genes of the histone 3 multigene family.
    Mol Biol Evol. 2002 Jan;19(1):68-75 PMID: 11752191
  51. The histone variant H3.3 regulates gene expression during lytic infection with herpes simplex virus type 1.
    J Virol. 2009 Feb;83(3):1416-21 PMID: 19004946
  52. Histone chaperone spt16 promotes redeposition of the original h3-h4 histones evicted by elongating RNA polymerase.
    Mol Cell. 2009 Aug 14;35(3):377-83 PMID: 19683500
  53. CHD1 motor protein is required for deposition of histone variant H3.3 into chromatin in vivo.
    Science. 2007 Aug 24;317(5841):1087-90 PMID: 17717186
  54. Histone H3.3 is enriched in covalent modifications associated with active chromatin.
    Proc Natl Acad Sci U S A. 2004 Feb 10;101(6):1525-30 PMID: 14732680
  55. Four histone variants mark the boundaries of polycistronic transcription units in Trypanosoma brucei.
    Genes Dev. 2009 May 1;23(9):1063-76 PMID: 19369410
  56. Epigenetic and replacement roles of histone variant H3.3 in reproduction and development.
    Int J Dev Biol. 2009;53(2-3):231-43 PMID: 19412883
  57. PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state.
    Mol Cell. 2006 Oct 20;24(2):309-16 PMID: 17052464
  58. Chromatin: sub out the replacement.
    Curr Biol. 2009 Jul 28;19(14):R545-7 PMID: 19640486
  59. Distinct factors control histone variant H3.3 localization at specific genomic regions.
    Cell. 2010 Mar 5;140(5):678-91 PMID: 20211137
  60. A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling.
    Cell. 2009 Jul 10;138(1):114-28 PMID: 19596239
  61. The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly.
    Mol Cell. 2002 Jun;9(6):1191-200 PMID: 12086617
  62. Drosophila GAGA factor directs histone H3.3 replacement that prevents the heterochromatin spreading.
    Genes Dev. 2007 Mar 1;21(5):552-61 PMID: 17344416
  63. Histone H3.3 variant dynamics in the germline of Caenorhabditis elegans.
    PLoS Genet. 2006 Jun;2(6):e97 PMID: 16846252
  64. The human and mouse replication-dependent histone genes.
    Genomics. 2002 Nov;80(5):487-98 PMID: 12408966
  65. Sin mutations alter inherent nucleosome mobility.
    EMBO J. 2004 Jan 28;23(2):343-53 PMID: 14726954
  66. The fission yeast HIRA histone chaperone is required for promoter silencing and the suppression of cryptic antisense transcripts.
    Mol Cell Biol. 2009 Sep;29(18):5158-67 PMID: 19620282
Article Info
Journal
Current opinion in genetics & development
Abbr.
Curr Opin Genet Dev
ISSN
1879-0380
DOI
10.1016/j.gde.2010.01.003
Email
selsaesser@rockefeller.edu
Published
2010-04-00
Epub
2010-00-12
Pages
110-7
Language
English
Region
England
NLM ID
9111375
PMCID
PMC2860041
Subset
IM
Grants
NIGMS NIH HHS · R01 GM040922 · United States
NIGMS NIH HHS · GM07739 · United States
NIGMS NIH HHS · R37 GM053512-30 · United States
NIGMS NIH HHS · R01 GM063959-08 · United States
NIGMS NIH HHS · R01 GM063959 · United States
NIGMS NIH HHS · R37 GM053512 · United States
NIGMS NIH HHS · T32 GM007739 · United States
NIGMS NIH HHS · T32 GM007739-31 · United States
NIGMS NIH HHS · R01 GM040922-25 · United States
External Links
PubMed source DOI: 10.1016/j.gde.2010.01.003 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2